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NOAA Technical Report NMFS 29 Prevalence, Intensity, Longevity, and Persistence of sp. Larvae and Lacistorhynchus tenuis Metacestodes in San Francisco Striped Bass

Mike Moser, Judy A. Sakanari, Carol A. Reilly, and Jeannette Whipple

April 1985

U.S. DEPARTMENT OF COMMERCE National Oceanic and Atmospheric Administration National Marine Fisheries Service NOAA TECHNICAL REPORTS NMFS

The major responsibilities of the National Marine Fisheries Service (NMFS) are to monitor and assess the abundance and geographic distribution of fishery resources, to understand and predict fluctuations in the quantity and distribution of these resources, and to establish levels for optimum use ofthe resources. NMFS is also charged with the development and implemen­ tation of policies for managing national fishing grounds, development and enforcement of domestic fisheries regulations, surveillance of foreign fishing off United States coastal waters, and the development and enforcement of international fishery agreements and policies. NMFS also assists the fishing industry through marketing service and economic analysis programs, and mongage insurance and vessel construction subsidies. It collects, analyzes, and publishes statistics on various phases of the industry. The NOAA Technical Repon NMFS series was established in 1983 to replace two subcategories of the Technical Reports series: "Special Scientific Repon-Fisheries" and "Circular." The series contains the following types of repons: Scientific investigations that document long-term continuing programs of NMFS, intensive scientific reports on studies of restricted scope, papers on applied fishery problems, technical repons of general interest intended to aid conservation and management, repons that review in considerable detail and at a high technical level cenain broad areas of research, and technical papers originating in economics studies and from management investigations. Copies of NOAA Technical Report NMFS are available free in limited numbers to governmental agencies, both Federal and State. They are also available in exchange for other scientific and technical publications in the marine sciences. Individual copies may be obtained from: U.S. Depanment of Commerce, National Technical Information Service, 5285 Port Royal Road, Springfield, VA 22161. NOAA Technical Report NMFS 29

Prevalence; --Intensi.ty; . )" '·1 ," .. '.... -. ' Lori'gevity, 'and Persistence Anis'akis~ P. of sp. 'Larvae.. and ."Lacisto'lhyh'chus teiniis" ., Metcicesfodes. in '; ." San Francisco Striped Bass

Mike Moser, Judy A. Sakanari, Carol A. Reilly, and Jeannette Whipple

April 1985

u.s. DEPARTMENT OF COMMERCE Malcolm Baldrige, Secretary National Oceanic and Atmospheric Administration John V. Byrne, Administrator National Marine Fisheries Service William G. Gordon, Assistant Administrator for Fisheries The National Marine Fisheries Service (NMFS) does not approve, recom­ mend or endorse any propriety product or proprietary material mentioned in this publication. No reference shall be made to NMFS, or to this publica­ tion furnished by NMFS, in any advertising or sales J'romotion which would indicate or imply that NMFS approves, recommends or endorses any proprietary product or proprietary material mentioned herein, or which has as its purpose an intent to cause directly or indirectly the advertised pro­ duct to be used or purchased because of this NMFS publication. CONTENTS

Introduction...... I Materials and methods ...... I Collection I Aging...... I Diet analysis ...... I Statistical analysis...... 1 Serial infections 1 Longevity and persistence...... 2 Results...... 2 Diet analysis ...... 2 Anisakis sp. 2 Host reaction...... 2 Prevalence and intensity...... 2 Serial infection ...... 2 Longevity and persistence...... 3 Lacistorhynchus tenuis ...... 3 Host reaction...... 3 Prevalence and intensity...... 3 Persistence...... 3 Other parasites and a tumor ...... 3 Discussion ...... 3 Acknowledgments...... 4 Literature cited ...... 4

Figures

1. Stomach content analysis of striped bass in the three major age groups in winter, spring, and summer...... 2 2. Cross section of posterior end of stomach with embedded larval 2 3. Prevalence and intensity of larval nematodes compared with age of host...... 2 4. Anisakis sp. larvae encapsulated in fibrous "raft" 3 5. Prevalence and intensity of metacestodes compared with age of host...... 3 6. Tumor, attached to mesenteries, cross section 3

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Prevalence, Intensity, Longevity, and Persistence of Anisakis sp. Larvae and Lacistorhynchus tenuis Metacestodes in San Francisco Striped Bass

MIKE MOSER, JUDY A. SAKANARI, CAROL A. REILLY,! and JEANNETTE WHIPPLE2

ABSTRACT

Thirteen hundred and seventy-three striped bass, Marone saxatilis, were collected from the San Francisco Bay-Delta area to correlate host diet with parasitic infections and to determine the prevalence, intensity, longe­ vity, and persistence of larval Anisakis sp. nematodes and the metacestode Lacistorhynchus tenuis. There is an in­ crease in the prevalence and intensity ofAIli.

INTRODUCTION Diet Analysis

Striped bass, Morone saxatilis, is a popular sportfish in the San The stomach contents of the fish were analyzed to determine Francisco Bay, CA, area. Anglers have often reported the presence' possible correlations between diet and parasite infections. of parasites in the mesenteries and muscle of striped bass and Stomach contents of 831 striped bass collected between January questioned the public health aspects of the parasitic infections. and September 1981 from San Pablo Bay and Suisun Slough were The purpose of this study was to determine the prevalence (no. examined for possible intermediate hosts. The Index of Relative hosts infected/no. hosts examined), intensity (total no. parasite's/ Importance (IRI) of items was determined by methods sug­ no. infected hosts), longevity (time parasites remain alive), and gested by Cailliet (1976). The young-of-the-year (YOY) and most persistence (time degenerated parasites are detectable) of the two of the l-yr-olds had similar diets, hence were combined for most c0mmonly seen parasites: the metacestode Lacistorhynchus analysis. The age groups for diet analysis were: YOY and l-yr-old tenuis () and the larval Anisakis sp. (probably A. (10 to 230 mm SL); subadult females and adult males (2 to 3 yr); simplex). am! adults (4+ yr).

MATERIALS AND METHODS Statistical Analysis

Collection The coefficient of dispersion (overdispersed distribution) was determined to indicate possible clumping in parasite distributions, Thirteen hundred and seventy-three striped bass were collected hence the possible need for nonparametric analysis (Sokal and from the San Francisco Bay-Delta area between June 1979 and Rohlf 1969). Within each age class seasonality did not signifi­ December i 983 by hook and line, gill net, and otter trawl. Fish cantly change the prevalance or intensity of the parasitic infec­ were frozen or Formalin-fixed and autopsied for parasites and tions. Therefore, all seasons were combined within each age class stomach content analy~es at Long Marine Laboratory, University (ANOYA, regression analysis). of California, Santa Cruz. Serial Infections Aging Serial'infections were performed to determine whether nema­ The age of the fish was determined by scale ring counts by the tode larvae can be transferred from fish to fish. The striped bass California Department of Fish and Game and the use of growth used in both infection experiments were YOY hatchery fish pro­ curves. vided by the California Department of Fish and Game, Elk Grove, CA. The third stage larval Ar;isakis sp. used were from bocaccio, Sebastes paucispinis. The fish were force-fed (Wootten and Smith 1975) with washed iarvae (Tanaka and Torisu 1978). Fifty larvae ICoastal Marine Studies, University of California, Santa Cruz, Santa Cruz, CA were fed to each of six striped bass. As a control, four YOY 95064. 'Physiological Ecology Investigations, Southwest Fisheries Center Tiburon yellowtail rockfish, Sebastes flavidus, were infected in a similar Laboratory, National Marine Fisheries Service, NOAA, Tiburon, CA 94920. manner. Longevity and Persistence

Striped bass collected from the field were observed to have degenerated larval nematodes in their mesenteries and tissues. The purposes of this experiment were to determine how long the larval Anisakis sp. remain alive in striped bass, therefore potentially harmful to humans, and to determine the persistence of dead lar­ vae in the mesenteries and muscle. The third stage Anisakis sp. lar­ vae used were prepared as above but were from sablefish, Anoplo­ poma fimbria. To insure that all fish were infected with equal numbers of larvae, 25 larvae were inserted into the coelomic cavi­ ty through a small cut on the sides of 178 striped bass. This wound was sealed with a nontoxic biological glue, Histoacryl (Tri-Hawk, Los Angeles, CAl. Previous tests showed that striped bass reacted similarly to larvae infected by this technique, to those force-fed, and to those seen in field fish. The hosts were periodically autop­ s'ed during a 33-wk period.

RESULTS Figure 2.-Cross section of posterior end of stomach with embedded larval nematodes. Diet Analysis

The fullness of the stomachs and the percent IRI for the domi­ nant food item or items are given for each age class. No stomachs contained larvae or metacestodes (Fig. I). I 60 [ 60 Anisakis sp. 0 u ~ '"z ·40 40 t:: '"...J

~ ~ masses of fibrous tissue. When several larvae were in close prox­ ace Ii imity in the mesenteries, they were often encapsulated to form a Years 'lOY 2 3 4 5 6 7 8 -- 76 fibrous "raft." In field fish with high intensity infections, 748 44 79 133 72 70 37 37 numerous degenerated larvae were found embedded in the posterior end of the stomach (Fig. 2). Figure 3.-Prevalence and intensity of larval nematodes compared with age of host. Bar =standard error. Prevalance and intensity.-The prevalence and intensity of larval nematode infections in striped bass begin to increase at 4 yr and continue to increase throughout the life uf the host. The mean Although the larvae from the striped bass responded weakly to to variance ratios (year classes 3 to 8+ are: 1.3,14.2,58.8,33.7, tactile stimuli, the cuticle had darkened, resembling the dead lar­ <19.9, 39.5, respectively) show the infections to be increasingly vae recovered from field-captured striped bass. In contrast, three overdispersed with time (Fig. 3). of the four rockfish were infected wIth an average of four larvae. The larvae from the rockfish were more active, and the cuticle Serial infection.-Autopsies showed that after 5 wk, two of six was flesh colored, similar to larvae from field-collected Sebastes striped bass were infected by one and four larvae. respectively. paucispinis and other fish hosts.

Neomysis sp. 100[L[]FiShes - 100til]-I ~ 50 i 50 a'i o o Neomysis sp 100 Fishes 5mol:

ll:: 10°[[I-'1 50 I :so1 a'i 0 ~ O~, 1::]1.-_-'-=__'--__

~IOot=o=J 100} c 100b :; 50 50 . LL ~:CLLJ g!!. 0 o ~ Figure I.-Stomach content analysis of striped bass in the three w Sp Su w Sp Su w Sp Su major age groups in winter (W), spring (Sp), and summer (Su). N= 109 :44 269 12 17 12 28 212 23 YOY-Iyr 2-3 yr 4+ yr

2 Longevity and persistence.-At the end of 2 wk most larvae 100 140 had been encapsulated into a fibrous "raft." In the following 31 wk, in addition to the "raft," one to five larvae were recovered in 120 the coelom or attached to the mesenteries. These larvae usually 60 responded weakly to tactile stimuli, but became progressively I00 darker and weaker with time (Fig. 4). I 60 0 w 60 (.) z >- W >- ...J 60 U) ~ 40 z w w a: >- n. 40 ~

20 20 Fl ~ Ylar. YOY 2 3 4 5 6 7 >8 N 748 44 79 76 133 72 70 37 37

Figure 5.-Prevalence and intensity of metacestodes compared with age of host. Bar = standard error.

(this study); -Stephanostomum tenue (D. Woodbury foot­ note 3), Lepocreadium californianum (Edwards and Nahhas 1968); -Cleidodiscus pricei (Hensley and Nahhas 1975); Nematoda-Thynnascaris brachyurum (as b., Hensley and Nahhas 1975), Spiroxys sp. (Hensley and Nahhas 1975), and Phocanema sp. larvae, in mesenteries, (this Figure 4.-Anisakis sp. larvae encapsulated in fibrous "raft." study); a tumor, in coelom, (this study, Fig. 6, National Museum of Natural History-Registry of Tumors in Lower (NMNH­ RTLA) #3173). Lacistorhynchus tenuis

Host reaction.-Moser, Sakanari, Wellings, and Lindstrom (1984) described the inflammatory response of the striped bass to these "rafts." The metacestodes from field fish appeared degen­ erated. The outer surface of the blastocyst was brown and the metacestode was a hardened mass. Often, the metacestodes, similar to the nematode larvae, were encapsulated into fibrous "rafts."

Prevalance and intensity.-During the first year the preva­ lence of larval cestode infections reached 81.6% and remained approximately at this level throughout the year. However, the mean intensity of infection slowly increases with the age of the Figure 6.-Tumor aJ allached to mesenteries, bJ cross section. host. The mean to variance ratios (age classes YOY to 8+ are: 14.4,23.2,38.9,9.2,48.6,36.7,59.3,51.2, 73.0, respectively) in­ dicate the infections were increasingly overdispersed with time DISCUSSION (Fig. 5). The food habits of San Francisco Bay-Delta striped bass have Persistence.-Four field fish kept in the laboratory for 22 mo been reported by Turner and Kelley (1966), Thomas (1967), Orsi still retained their dead metacestodes and "rafts." (1971), Moriguchi (1973), Moyle (1976), and Orsi and Knutson (1979). The present study and the above reports show that YOY Other Parasites and a Tumor consume primarily shrimp (Neomysis sp. and Crangon sp.), amphi­ pods (Corophium sp.), and copepods. By the end of the first year Occasionally other helminth parasites were encountered during the fish begin to switch from feeding on to eating autopsies. However, because of the overall goal of this study and fish (striped bass, shad, , flatfish, , perch, bait). This the method of preservation of field fish, no attempt was made to trend continues in the subadults. Although adults are primarily quantify these helminths. Parasites reported from the San Fran­ piscivorous, striped bass continue to eat some invertebrates, such cisco Bay-Delta include: -Southwellina (D. as crabs. The adults, and perhaps the subadults, reduce their feed­ WoodburyJ); Cestoda-Tetraphyllidae larvae, in mesenteries, ing in the spring and early summer during the spawning season. The life cycle of Anisakis sp. usually includes a marine crusta­ cean as the first intermediate host, a fish or squid as the second 3D. Woodbury, Seasonal Aide, California Department of Fish and Game, 203 Tall host, and a marine as the definitive host. The larva of Trees Drive, Vallejo, CA 94589, pers. commun. March) 983. Anisakis sp. is well known as a potential hazard to human health if

3 consumed in raw or improperly prepared seafood (Moser, Love, Santa Cruz, and the National Marine Fisheries Service, Tiburon, and Sakanari 1984). San Francisco Bay striped bass infected with CA; Marvin Jung, State Water Resources Control Board; Frank larval Anisakis do not appear to be a major health hazard. Rarely Fisher and the California Department of Fish and Game, Kinne­ were these larvae found in the muscle tissue. In addition, most of tics Laboratory; Elmer Noble, University of California, Santa Bar­ the larvae degenerate in the body cavity after a few weeks. The bara; James Berry, Scripps Institute of Oceanography, La Jolla, results of this study suggest that some degenerating larvae and the CA; Donald Gruber, Pinole, CA; Thomas Tucker, Steinhart Aqua­ fibrous "rafts" can persist in striped bass for at least 33 wk. This rium, California Academy of Sciences. slow turnover rate of larvae probably contributes to the increase in intensity of infection with time. LITERATURE CITED Wootten and Smith (1975) showed that trout can be serially infected with Anisakis sp. larvae from herring. Many of the fish CAILLlET, G. M. consumed by striped bass are infected by Anisakis sp. larvae (Love 1976. Several approaches to the feeding ecology of fishes. First Pac. N.W. T~ch. Workshop. Sess. 1. Workshop Proc., Astoria, Oreg., October 13-15, and Moser 1983). The serial infection experiments with Anisakis 1976, sp. larvae may explain the increase in prevalence and intensity as EDWARDS, S. R., and F. M. NAHHAS. striped bass become more piscivorous at 4 yr. Although numerous 1968. Some endoparasites of fishes from the Sacramento-San Joaquin Delta, fibrous "rafts" were found in the mesenteries and next to the California. Calif Fish Game 54:247-256. HENSLEY, G. H., and F. M. NAHHAS, peritoneum of field fish, they did not form open lesions as describ­ 1975. Parasites of fishes from the Sacramento-San Joaquin Delta, California, ed for the metacestodes of L. tenuis in San Francisco Bay striped Calif. Fish Game 61 :20 1-208. bass (Moser, Sakanari, Wellings, and Lindstrom 1984). LOVE, M. S., and M. MOSER. The life cycle ofLacistorhynchus tenuis, although not complete­ 1983. A checklist of parasites of California, Oregon, and Washington marine ly described, most probably includes the adult in an elasmo­ and estuarine fishes. U.S. Dep. Commer., NOAA Tech. Rep. NMFS SSRF­ 777, 576 p. branch, such as the leopard , Triakis semifasciata, common to MORIGUCHI, M. N. San Francisco Bay, the procercoid in a , and the meta­ 1973. Food habits of the striped bass, Roccus saxalilis, (Walbaum) in San cestode in fish. Lacistorhynchus tenuis metacestodes have been Francisco Bay with notes on the major areas of the fishery. M.A. Thesis, reported worldwide from more than 60 species of hosts (Moser San Francisco State Univ., San Francisco, CA, 61 p. MOSER, M. 1983), including striped bass from the east coast and other San 1983. Parasites of San Francisco Bay-Delta area stripped bass (Morone Francisco Bay fish, with no apparent harm to the host. However, saxatilis) and other San Francisco Bay fishes. Final Rep., Calif. State Water Moser, Sakanari, Wellings, and Lindstrom (1984) have shown Res. Control Board, Sacramento, CA, I 14 p. that these metacestodes are pathological to striped bass found in MOSER, M., M. LOVE, and 1. SAKANARI. the San Francisco Bay-Delta area. 1984. Common parasites of California fishes. Calif. Dep. Fish Game, 20 p. MOSER, M., J. SAKANARI, S. WELLINGS, and K. LINDSTROM. The sharp rise in prevalence of L. tenuis metacestodes in the 1984. Incompatibility between San Francisco striped bass, Marone saxa/ilis l-yr-olds may be related to the movement of this age class from (WalbaumJ, and the metacestode, Lacislorhynchus lenuis (Beneden 1858). the Delta area into San Francisco Bay where they are more 'likely 1. Fish Dis. 7:397-400. to encounter the infected intermediate hosts. The continued in­ MOYLE, P. B. 1976. Inland fishes of California. Univ. Calif. Press, Berkeley, 405 p. crease in the intensity of metacestodes through time may reflect ORSI, J. J. both the acquisition of new metacestodes and their persistence in 1971. The 1965-1967 migrations of the Sacramento-San Joaquin Estuary the host. Preliminary studies (Sakanari, Moser) suggest that meta­ striped bass population. Calif Fish Game 57:257-267. cestodes ofL. tenuis can be transfered serially from white croaker, ORSl, J. J.. and A C. KNUTSON. Genyonemus lineatus, to striped bass. These studies suggest that 1979, The role of mysid shrimp in the Sacramento-San Joaquin estuary and factors affecting their abundance and distribution. In T. J. Conomos (editor), the prevalence of metacestodes from the YOY to the I yr class San Francisco Bay: The urbanized estuary, p. 401-408. Pac. Div.lA.A.A.S., may also be related to increased piscivory. The increased clumped San Francisco State Univ., CA, June 12-16, 1977. distribution of parasites with the age of the host may indicate SOKAL, R. R., and F. J. ROHLF. striped bass vary in their susceptibility to these parasites. Some 1969. Biometry. The principles and practice of statistics in biological research. W. H. Freeman and Co., San Francisco, CA, 776 p. hosts may eliminate the parasites before they can become embed­ TANAKA, 1., and M. TORISU. ded in the mesentaries or muscle tissue. Striped bass were intro­ 1978. Anisakis and eosinophil. I. Detection of a soluble factor selectively duced into San Francisco Bay from the east coast approximately chemotactic for eosinophils in the extract from Anisakis larvae. J.lmmunol. 100 yr ago. The type of incompatibility shown here has not been 120:745-749. described between east coast striped bass and their helminth THOMAS, 1. L. 1967. The diet of juvenile and adult striped bass, Roccus saxalilis, in the parasites. Current studies are investigating the possibility that the Sacramento-San Joaquin River system. Calif. Fish Game 53:49-62. west coast striped bass are immunologically incompatible with the TURNER, J. L., and D. W. KELLEY. indigenous strain of parasite. 1966. Ecological studies of the Sacramento-Joaquin Della. Calif. Dep, Fish Game, Fish Bull. 136, Part II, Fishes of the Delta, 168 p. WOOTTEN, R., and J. w. SMITH. ACKNOWLEDGMENTS 1975. Observational and experimental studies on the acquisition of Anisakis sp. larvae (Nematoda: ) by trout in fresh water. Int. J. Parasitol. We thank the staffs at Marine Studies, University of California, 5:373-378.

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